Research

Gamete compatibility and

Speciation in Arctic sea urchins

Selective forces that shape the evolution of gamete morphology are
complex, and the links between gamete morphology, reproductive isolation and
genetic divergence remain elusive.In
marine invertebrates, positive selection on reproductive traits is thought to
drive the rapid divergence of sperm and egg proteins. Likewise, sexual
selection has been implicated in the evolution of egg size and egg accessory
coats. A similar role has been suggested for sperm morphology but while basic
sperm morphology has been described for many marine invertebrates, few data
exist on within species variation in sperm traits, and the underlying genetic
architecture remains to be examined. Unraveling the consequences and adaptive
significance of within-species variation in sperm morphology and its pattern
among free-spawning invertebrates may help elucidate the evolution of
reproductive isolation, and thus the mechanisms that underlie the formation of
new marine species.

Together with collaborators, I document among-population variation in sperm morphology that is correlated with population divergence in neutral genetic markers, and possibly with adaptive features of reproductive compatibility. This is an expanding area, especially in echinoderms in which it's possible to assay variation in gamete compatibility in vitro and parallel variation at some of the loci that encode gamete recognition molecules. Combined with the use of microsatellites for paternity analysis (allowing for experimental investigations into, for example, sperm precedence among individuals and species), this is a tractable system for enquiries into the genetic basis of species recognition, species-specific gamete traits and life-history evolution. Comparing adaptive traits within and among species and populations from different oceans andlatitudes– from temperate to high arctic ecosystems, allows for results to be interpreted in the context of adaptation to climate change, in addition to testing theoretical evolutionary models.

In other
work, I empirically test current theory on egg-size evolution and the role of
gamete traits and sperm availability.Here, we directly address an ongoing controversy
about the effect of egg-accessory coats on fertilization success and egg-size
evolution, and thus the evolution of anisogamy.

Strongylocentrotus droebachiensis shows spectacular intraspecific variation in egg size with latitude
along the Norwegian coast, and variation in egg jelly-coat thickness that is
inversely proportional to egg size.We
use this geographic gradient to experimentally test the combined effects of egg
and accessory-coat size on fertilization success.We show that the 'egg fertilizability' (the
chance that a sperm will fertilize an egg if it encounters one) varies with
target size and sperm concentration, and thus that the sea urchin system
violates an assumption of the most widely used model of fertilization
kinetics.We suggest the need to
incorporate into existing fertilization kinetics models the interactions
between egg size, total target size, and accessory-coat thickness, and how
these vary with sperm concentration.

In
free-spawning organisms, the risk of both incomplete fertilization (related to
sperm limitation) and lethal fertilization by more than one sperm (under conditions
of sperm competition) may influence the evolution of traits related to
fertilization success.Given increasing evidence
for great environmental heterogeneity in sperm concentration during natural
spawning events, we provide evidence that studies of fertilization dynamics in
free-spawning organisms should consider the role of egg-accessory coats in
terms of a possible tradeoff between egg size and total target size and its
complicated relationship to sperm.

Population genetics

Photo: C. Biermann
Understanding marine population connectivity is
critical for sustainable management of marine resources. The degree to which
populations of marine organisms exchange migrants determines whether they
function as one large metapopulation or many independent units and thus
influences their response to potential disturbance from harvesting, habitat
destruction or climate change. As such, knowledge of connectivity directly
impacts management decisions and addresses the question of whether fisheries
management and the design of marine protected areas should be tailored to
variation in coastal geography and regional oceanographic conditions.

It is often assumed that marine species with
long-lived planktonic larvae disperse great distances in ocean currents and will
thus exhibit low levels of genetic differentiation. However, recent evidence shows
that significant population-genetic subdivision may occur even in species with
a long larval duration and that variability in ocean currents can influence the
spatial genetic structure of marine populations.

We are presently working to determine the population
genetic structure of the sea urchins Strongylocentrotus
droebachiensis and Strongylocentrotus
pallidus along the Norwegian coast and Svalbard,
using a fragment of the cytochrome c
oxidase I gene (COI) of the mitochondrion and microsatellite assays. Is there
genetic differentiation of separate populations, or clinal variation within
genetically continuous populations? How do these populations compare to samples
from Greenland, the eastern Pacific and
western Atlantic oceans?

The common green sea urchin, Strongylocentrotus droebachiensis has a circumarctic distribution,
and shows substantial genetic subdivision between northeastern Atlantic
populations and northwestern Atlantic and
Pacific populations (Marks et al. 2004). Norwegian populations show significant
divergence from their Pacific counterparts in both mitochondrial DNA (Addison and
Hart, 2005) and
nuclear DNA (sperm bindin: Marks et al. 2008; microsatellites: Addison and
Hart, 2004; 2005).Little is known,
however, about fine-scale populations subdivisions within these regions. The
high degree of genetic divergence among S.
droebachiensis populations (> 1.5% in bindin; 3.5% in mtDNA) is in fact greater
than that separating several species pairs of Indo-West Pacific sea urchins (0.9%; Landry et al., 2003).Northwestern Atlantic S. droebachiensis populations contain a mixture of alleles from
both northern Pacific and European sources (Addison and
Hart, 2004; 2005; Harper et al.,
2007; Palumbi and Wilson, 1990).Fine-scale genetic sampling of S. droebachiensis from the Arctic and
northwest Atlantic will shed light on how
populations of this species have evolved.

Throughout their geographic range, these urchins
exhibit differences in life-history traits including egg size, larval duration
and size at metamorphosis (Biermann et al. 2004; Marks, unpublished data). Egg
size increases 4-fold in volume along a latitudinal gradient from Sweden to
Spitzbergen. Likewise, sperm morphology differs markedly among populations of S. droebachiensis from different oceans,
and reflects patterns of genetic divergence (Marks et al. 2008), yet the
underlying genetic architecture of these traits remains enigmatic. There is
also marked variation in the strength of reproductive barriers (fertilization
success) between populations and oceans (Marks and Biermann, unpublished data)
and between S. droebachiensis and S. pallidus from different populations
(Biermann and Marks 2000).

In many marine fish, both adults and larvae contribute
to migration among populations. Sea urchins have benthic adults with relatively
little mobility, and population genetic structure will be determined by the
interaction of regional oceanographic conditions and life-history traits. As
such, the sea urchin system provides a proxy for dispersal of other commercially
important organisms with pelagic larvae along the Norwegian coast and Svalbard.
This study contributes knowledge of sea urchin population structure
that is critical in managing natural populations of urchins and kelp
forests and prerequisite for a sustainable commercial urchin fishery
developing in Norway today.